Gut Microbiota Alterations in Adolescent Idiopathic Scoliosis Are Associated with Aberrant Bone Homeostasis
Objective Low bone mineral density is the major prognostic factor for adolescent idiopathic scoliosis (AIS), but the underlying mechanisms remain unclear. Accumulating evidence suggests that gut microbiota (GM) have the potential to affect bone development, and the GM signatures are altered in AIS p...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Wiley
2024-04-01
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| Series: | Orthopaedic Surgery |
| Subjects: | |
| Online Access: | https://doi.org/10.1111/os.14019 |
| _version_ | 1797231097267879936 |
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| author | Jie Li Changwei Liu Yanjie Xu Chen Ling Ziyang Tang Abdukahar Kiram Zongshan Hu Zezhang Zhu Yong Qiu Zhen Liu |
| author_facet | Jie Li Changwei Liu Yanjie Xu Chen Ling Ziyang Tang Abdukahar Kiram Zongshan Hu Zezhang Zhu Yong Qiu Zhen Liu |
| author_sort | Jie Li |
| collection | DOAJ |
| description | Objective Low bone mineral density is the major prognostic factor for adolescent idiopathic scoliosis (AIS), but the underlying mechanisms remain unclear. Accumulating evidence suggests that gut microbiota (GM) have the potential to affect bone development, and the GM signatures are altered in AIS patients. However, the effect of GM alterations on aberrant bone homeostasis in AIS remains unclear. This study aims to investigate the GM profile in AIS patients with different bone mineral density (BMD) and explore the association between GM, osteopenia, and aberrant bone turnover. Methods A total of 126 patients with AIS who received surgical treatment were retrospectively included in this study. We analyzed the composition of the GM by 16S rRNA sequencing and BMD by dual X‐ray absorptiometry. Based on the BMD of the femur neck, the patients were divided into the osteopenia group (OPN) if the Z score < −1, and the normal (NOR) group if the Z score ≥ −1 SD compared to the healthy control. For the 16S rRNA sequencing, the raw reads were filtered to remove low‐quality reads, and operational taxonomic units were identified with the Uparse program. Weighted UniFrac distance matrix for the beta‐diversity metrics and principal coordinate analysis (PCoA) was performed, and the statistical comparisons were made with permutational multivariate analysis of variance (PERMANOVA) and analysis of similarity (ANONISM). Linear discriminant analysis effect size (LEfSe) was used to identify the enriched species in two groups. The “Random forest” was applied to determine the optimal biomarker for OPN according to the mean decrease in Gini value. The metabolic function was predicted by the Tax4Fun analysis. The Pearson correlation coefficient was used to evaluate the associations between GM species, bone turnover markers, and BMD. Results The serum β‐CTX was increased in the OPN group (n = 67) compared to the NOR group (n = 59). Patients in OPN groups showed significantly decreased α diversity indicated by the Shannon index. Principal coordinate analysis (PCoA) analysis showed significant clustering of GM between OPN and NOR groups. At genus level, the Escherichia‐Shigella and Faecalibacterium were significantly enriched in the OPN group compared to that in the NOR group (p < 0.05), whereas the abundance of Prevotella was significantly decreased (p = 0.0012). The relative abundance of Megamonas and Prevotella was positively correlated with the femur BMD. The abundance of Escherichia‐Shigella was negatively correlated with femur BMD and positively correlated with serum β‐CTX levels. Functional analysis revealed significant differences in starch and sucrose metabolism, pyruvate and cysteine, and methionine metabolism between NOR and OPN groups. Conclusion The alterations of GM in AIS patients are correlated with osteopenia. The association between enriched species, BMD, and bone turnover markers provides novel diagnostic and therapeutic targets for the clinical management of AIS. |
| first_indexed | 2024-04-24T15:38:58Z |
| format | Article |
| id | doaj.art-d7c1555434da41a3b35d39e80b2e5169 |
| institution | Directory Open Access Journal |
| issn | 1757-7853 1757-7861 |
| language | English |
| last_indexed | 2024-04-24T15:38:58Z |
| publishDate | 2024-04-01 |
| publisher | Wiley |
| record_format | Article |
| series | Orthopaedic Surgery |
| spelling | doaj.art-d7c1555434da41a3b35d39e80b2e51692024-04-02T01:03:25ZengWileyOrthopaedic Surgery1757-78531757-78612024-04-0116496597510.1111/os.14019Gut Microbiota Alterations in Adolescent Idiopathic Scoliosis Are Associated with Aberrant Bone HomeostasisJie Li0Changwei Liu1Yanjie Xu2Chen Ling3Ziyang Tang4Abdukahar Kiram5Zongshan Hu6Zezhang Zhu7Yong Qiu8Zhen Liu9Division of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, Clinical College of Nanjing Medical University Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, Clinical College of Nanjing Medical University Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, Clinical College of Nanjing Medical University Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School Nanjing ChinaDivision of Spine Surgery, Department of Orthopedic Surgery Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School Nanjing ChinaObjective Low bone mineral density is the major prognostic factor for adolescent idiopathic scoliosis (AIS), but the underlying mechanisms remain unclear. Accumulating evidence suggests that gut microbiota (GM) have the potential to affect bone development, and the GM signatures are altered in AIS patients. However, the effect of GM alterations on aberrant bone homeostasis in AIS remains unclear. This study aims to investigate the GM profile in AIS patients with different bone mineral density (BMD) and explore the association between GM, osteopenia, and aberrant bone turnover. Methods A total of 126 patients with AIS who received surgical treatment were retrospectively included in this study. We analyzed the composition of the GM by 16S rRNA sequencing and BMD by dual X‐ray absorptiometry. Based on the BMD of the femur neck, the patients were divided into the osteopenia group (OPN) if the Z score < −1, and the normal (NOR) group if the Z score ≥ −1 SD compared to the healthy control. For the 16S rRNA sequencing, the raw reads were filtered to remove low‐quality reads, and operational taxonomic units were identified with the Uparse program. Weighted UniFrac distance matrix for the beta‐diversity metrics and principal coordinate analysis (PCoA) was performed, and the statistical comparisons were made with permutational multivariate analysis of variance (PERMANOVA) and analysis of similarity (ANONISM). Linear discriminant analysis effect size (LEfSe) was used to identify the enriched species in two groups. The “Random forest” was applied to determine the optimal biomarker for OPN according to the mean decrease in Gini value. The metabolic function was predicted by the Tax4Fun analysis. The Pearson correlation coefficient was used to evaluate the associations between GM species, bone turnover markers, and BMD. Results The serum β‐CTX was increased in the OPN group (n = 67) compared to the NOR group (n = 59). Patients in OPN groups showed significantly decreased α diversity indicated by the Shannon index. Principal coordinate analysis (PCoA) analysis showed significant clustering of GM between OPN and NOR groups. At genus level, the Escherichia‐Shigella and Faecalibacterium were significantly enriched in the OPN group compared to that in the NOR group (p < 0.05), whereas the abundance of Prevotella was significantly decreased (p = 0.0012). The relative abundance of Megamonas and Prevotella was positively correlated with the femur BMD. The abundance of Escherichia‐Shigella was negatively correlated with femur BMD and positively correlated with serum β‐CTX levels. Functional analysis revealed significant differences in starch and sucrose metabolism, pyruvate and cysteine, and methionine metabolism between NOR and OPN groups. Conclusion The alterations of GM in AIS patients are correlated with osteopenia. The association between enriched species, BMD, and bone turnover markers provides novel diagnostic and therapeutic targets for the clinical management of AIS.https://doi.org/10.1111/os.14019Adolescent idiopathic scoliosisBone turnoverGut microbiotaOsteopenia |
| spellingShingle | Jie Li Changwei Liu Yanjie Xu Chen Ling Ziyang Tang Abdukahar Kiram Zongshan Hu Zezhang Zhu Yong Qiu Zhen Liu Gut Microbiota Alterations in Adolescent Idiopathic Scoliosis Are Associated with Aberrant Bone Homeostasis Orthopaedic Surgery Adolescent idiopathic scoliosis Bone turnover Gut microbiota Osteopenia |
| title | Gut Microbiota Alterations in Adolescent Idiopathic Scoliosis Are Associated with Aberrant Bone Homeostasis |
| title_full | Gut Microbiota Alterations in Adolescent Idiopathic Scoliosis Are Associated with Aberrant Bone Homeostasis |
| title_fullStr | Gut Microbiota Alterations in Adolescent Idiopathic Scoliosis Are Associated with Aberrant Bone Homeostasis |
| title_full_unstemmed | Gut Microbiota Alterations in Adolescent Idiopathic Scoliosis Are Associated with Aberrant Bone Homeostasis |
| title_short | Gut Microbiota Alterations in Adolescent Idiopathic Scoliosis Are Associated with Aberrant Bone Homeostasis |
| title_sort | gut microbiota alterations in adolescent idiopathic scoliosis are associated with aberrant bone homeostasis |
| topic | Adolescent idiopathic scoliosis Bone turnover Gut microbiota Osteopenia |
| url | https://doi.org/10.1111/os.14019 |
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